Botanical Sources and Sugar Concentration of the Nectar Collected by Two Stingless Bee Species in a Tropical African Rain Forest*

Apidologie 38 (2007) 110–121 110 c INRA/DIB-AGIB/ EDP Sciences, 2007 DOI: 10.1051/apido:2006051 Original article

Botanical sources and sugar concentration of the nectar collected by two stingless bee species in a tropical African rain forest*

Robert Ka, b

a Faculty of Biology, Department of Behavioural Biology, Tropical Bee Research Unit, PO Box 80.086, 3508 TB Utrecht, The Netherlands b Permanent Address: Department of Forest Biology and Ecosystems Management, Faculty of Forestry and Nature Conservation, Makerere University, PO Box 7062, Kampala, Uganda

Received 3 January 2005 – Revised 15 October 2005 – Accepted 10 August 2006

Abstract – Nectar foraging by species of two stingless bees was studied in an African tropical rain forest. Both species Hypotrigona gribodoi (2–3 mm) and Meliponula ferruginea (6 mm) collected nectar with a wide range of sugar concentration (H. gribodoi: 14.2–67.4%; M. ferruginea: 9.1–63.4%). H. gribodoi collected nectar of higher sugar concentration than M. ferruginea. Factors that inﬂuenced sugar concentration of collected nectar included botanic origin of the nectar, bee species, bee colonies, month of year, time of day and the local environment. Sugar concentration increased gradually from 0700 h to a peak at 1300 h and declined thereafter. H. gribodoi collected nectar from more diverse plant species than M. ferruginea. Sugar concentration for both bee species was higher during the dry season than the rainy season. Although the above factors may explain part of the variation in the sugar concentration of nectar, additional explanations lie in the behavioural diﬀerences among the bee species.

nectar concentration / nectar sources / Calliandra calothyrsus / foraging behaviour / Budongo Forest Reserve

1. INTRODUCTION qualities and quantities presented by plants (Roubik, 1989; Biesmeijer et al., 1999b). Several species of stingless bees can oc- Flower visitors can differentiate between the cur sympatrically and their diets partly over- amount of nectar in flowers, its sugar concen- lap permitting access to the same resources tration, and its composition in sugars, amino by many colonies (Sommeijer et al., 1983; acids and lipids (Baker and Baker, 1975, 1983; Roubik et al., 1986; Kleinert-Giovanini and Opler, 1983; Roubik and Buchmann, 1984; Imperatriz-Fonseca, 1987; Ramalho et al., Roubik et al., 1995; Biesmeijer and Ermers, 1989; Ramalho, 1990; Roubik et al., 1995; 1999). Kajobe and Roubik, 2006). The overlap in diet can lead to competitive interactions (Hubbel Honey bees have a preference mainly for and Johnson, 1977, 1978; Roubik and Aluja, those plants that provide a better reward, that 1983; Roubik, 1989). The competition for nec- is the largest amount of pollen, or nectar, or tar can result in the evolution of not only both, those having more concentrated nectar, morphological adaptations of both plants and and those that have not been foraged on pre- animals but also in a wide range of nectar viously by other bees (Roubik, 1989). Factors that cause variation in harvested nectar sugar Corresponding author: R. Kajobe, concentration include the botanical origin of [email protected] nectar, local climate, as well as behavioural * Manuscript editor: B. Vassière and J. Pierre differences among bee species and among Article published by EDP Sciences and available at http://www.edpsciences.org/apido or http://dx.doi.org/10.1051/apido:2006051 Nectar sources and sugar concentration for African stingless bees 111

Figure 1. Location of the Budongo Forest Reserve (DRC = Democratic Republic of Congo). colonies within the same species (Biesmeijer Studies are very limited on the floral origin et al., 1999b). These authors concluded that of nectar collected by African stingless bees. the variation of climatological conditions be- There has been no major study to fully explain tween patches might lead to heterogeneous the nectar foraging ecology of social bees in nectar rewards. African tropical rain forests. The patterns and ecological impact of floral choice and foraging Spatial and temporal niche differentiation behaviour of social bees in this environment between sympatric stingless bee species can are largely unknown. This study was there- arise by differences in bee morphology, for ex- fore aimed at answering the following ques- ample with body size, colour and mouth parts tions: what are the important nectar sources of (Biesmeijer et al., 1999a). Resource partition- stingless bees in the Budongo forest reserve? ing can also be the result of behavioural dif- What is their diversity? What factors influence ferences among bee foragers, for example the the sugar concentration of collected nectar, in timing of the foraging activity, the ability to particular is there an effect of the bee species recruit, the intrinsic collecting behaviour, ag- on the concentration of the nectar collected? A gressiveness, and the food selection (Frankie comparison between honey bees and stingless et al., 1976; Villanueva, 1994). Temporal re- bees was made in an effort to understand the source partitioning was described by Frankie ecology of their nectar foraging behaviour. et al. (1976) who found that the species composition of bee fauna foraging on a particular flower patch changed over the course of a day, 2. MATERIALS AND METHODS thus suggesting that differences in the timing of foraging may help to avoid direct compe- 2.1. Study site tition among species at flowers. In that study, they noted a tendency for larger bees to for- The main study was conducted in the Budongo age earlier in the day compared to the smaller Forest Reserve (BFR), which is a tropical rain for- species. est located in mid-western Uganda. It is an outlier of 112 R. Kajobe

the great Ituri forest of the Democratic Republic of Nectar was collected from foragers by forcing the Congo (Fig. 1). It covers an area of 825 km2,mak- bees to expel their crop load into a 20 µL capillary ing it Uganda’s biggest forest reserve (Hamilton, tube for the small bee, H. gribodoi and 50 µLfor 1984); 53% of it is continuous forest cover while M. ferruginea. In the case of H. gribodoi, samples the remaining comprises grassland communities. It from 2–3 bees were occasionally combined to ob- is located east of the Western rift valley escarp- tain more reliable sugar concentration values. Con- ment and Lake Albert between 1◦35’ and 1◦55’ centration of sugar (actually total dissolved solids) N, and 31◦18’ and 31◦42’ E (Howard, 1991). The in the nectar was measured with a hand refractome- forest lies at an average altitude of 1100 m (mini- ter corrected for ambient temperature (results ex- mum 750 m and maximum 1250 m) above sea level pressed in g per 100 g of solution). Bees carrying (Eggeling, 1947). loads with less than 5% in sugar concentration were ignored because they probably consisted mainly of water foragers (Roubik and Buchmann, 1984). Data 2.2. Bee colonies on ambient temperature was taken at each time of nectar collection. We used four natural nests of two stingless bee species, two colonies of Hypotrigona gribodoi and two of Meliponula ferruginea. These two species 2.4. Identification of nectar and pollen were selected because they represent the two gen- sources era of stingless bees that have been identified in Uganda. The colonies were located at most 80 m Nectar foragers carried pollen of different apart in various tree cavities close to the border of colours on different parts of their bodies. These the forest. The stingless bees were identified based pollen grains adhering to the body of the bees on Eardley (2004) and their identity was confirmed were sampled by trapping the bee with glycerine by David W. Roubik at Smithsonian Tropical Re- jelly and we analysed this pollen to identify the search Institute. Measurement of the bee sizes (dry nectar sources used by the bees. We obtained a body length) was recorded in the Royal Museum wide variety of samples by selectively sampling for Central Africa, Tervuren, Belgium, using an oc- foragers from each visually distinguishable pollen ular micrometer on a stereoscopic microscope. The colour type. Such a sampling method can cause smaller bee species, H. gribodoi (2–3 mm) is pale a slight overestimation of the diversity in nectar in colour. Two morphs of M. ferruginea (6 mm), diet (Biesmeijer et al., 1999b). Several representa- one black and the other brown have been identified tives of each colour of pollen were acetolysed and in Uganda. They were previously called Meliponula mounted in glycerine jelly for microscopic exam- erythra, but are now regarded as species synonyms ination (Sawyer, 1981). The colour and amount of (Eardley, 2004). The brown form is the one that ex- the pollen was recorded. Most slides contained only ists in Budongo forest reserve and was therefore one type of pollen and slides that contained more used in this study. than one type were not included in our analysis. The different pollen types were identified by making use of our reference collection and by consult- 2.3. Sampling and analysis of nectar ing Hamilton (1972). A nectar source was referred collected by H. gribodoi and to as a major source if it contributed at least 30% of M. ferruginea the samples from one colony during a day of observation. All other sources were referred to as minor From March to August 2002, nectar samples sources. were taken once a week from 10 returning foragers per colony, five times a day at 0600–0700 h, 0900– 1000 h, 1100–1200 h, 1300–1400 h and 1500– 2.5. Nectar collection from Calliandra 1600 h local time. The methods used were similar to calothyrsus by stingless bees and those used by Biesmeijer et al. (1999b). At the nest Apis mellifera entrances, returning nectar foragers were caught with a net. Nectar foragers carried pollen of dif- This second study was undertaken to provide ferent colours and on different parts of their bodies background data on the possible changes in the con- (but did not carry pollen loads in their corbiculae). centration of the crop content of the stingless bees Nectar sources and sugar concentration for African stingless bees 113

Table I. Nectar concentration collected by foragers from four colonies of two stingless bee species upon their return to the nest. Colony number Number of samples analyzed Minimum Maximum Mean Standard deviation Nectar concentration (g solute / 100 g solution) Melipona ferruginea 1 260 9.1 63.4 42.2 1.72 2 260 12.5 63.2 39.8 1.62 Hypotrigona gribodoi 1 313 14.2 67.4 43.7 1.56 2 313 15.1 63.4 43.2 1.43 between the flowers they foraged upon and their re- an Arcsine Square root Transformation (Sokal and turn to the nest. Also we included honey bees in this Rohlf, 1995). To report the means, the results were study to extend our sampling to three species of so- converted back to percentages. A nested ANOVA cial bees. Data were taken once a week from June was performed to determine the factors influencing to September 2002 on flower visitation and concen- sugar concentration of collected nectar. The model tration of collected nectar from C. calothyrsus (Mi- used was: mosaceae) by A. mellifera, H. gribodoi and M. fer- Nectar concentration = Bee species + Colony ruginea in Nyabyeya Forestry College agroforestry (bee species) + Month + Time of day + Month × demonstration farm. The farm was planted with Time of day + Bee species × Month + Bee species × about 5 ha of C. calothyrsus, a shrub that reached a Time of day + Bee species × Month × Time of height of 4–6 m and flowers throughout the year and day Colony (bee species) × Month + Colony (bee is a primary source of nectar for bees. Most flowers species) × Time of day + Colony (bee species) × open at 1600 h for a single night. Foragers were cap- Month × Time of day + error. Bee species, month tured immediately after imbibing nectar for an un- and time of day were treated as fixed factors while interrupted period. Nectar samples were taken once colony was considered random. Pearson correla- a week from 2–5 foragers of each bee species five tion coefficients were calculated to determine the times a day at 0600–0700 h, 0700–0800 h, 1600– relationship between the temperature and the con- 1700 h, 1700–1800 h and 1800–1900 h. These times were selected in relation to the observed period centration of collected nectar. The average diver- of anthesis of C. calothyrsus in the agro-forestry sity of pollen types per nest was calculated using = Σ farm. The same methods, as previously described a Shannon-Weaver index of diversity: H’ik – j / Σ / Σ in 2.3 and 2.4, were used to extract the crop con- [{Nijk j (Nijk)} ln {Nijk j (Nijk)}] in which H’ik tent from the bees and identify the nectar sources is Shannon-Weaver’s index of colony i, over one respectively. There was little chance the nectar thus month k and N is the number of pollen types. In- sampled came from other flower species or colony dices were calculated for each colony per month stores, since floral constancy of stingless bees is and thereafter averaged. Kruskal-Wallis tests were quite high (Slaa et al., 1998). The time taken to carried out to compare the nectar handling time and visit one flower and five flowers in succession was foraging speed on Calliandra calothyrsus. recorded for some selected individual bees to determine the handling time and foraging speed for the three bee species gathering nectar on C. calothyr- 3. RESULTS sus. 3.1. Sugar concentration of collected 2.6. Data analysis nectar

The main dependent variable in this study was The two stingless bee species H. gri- the sugar concentration of the crop content ex- bodoi and M. ferruginea collected nectar pressed as gram (g) of solute per 100 g of solu- with a wide range of sugar concentrations tion. These percentages ranged from 9.1 and 67.4%, (H. gribodoi: 14.2–67.4%; M. ferruginea:9.1– and so the data was analyzed as proportion after 63.4%; Tab. I). Overall, H. gribodoi collected 114 R. Kajobe

Figure 2. Compared sugar concentration of nectar collected by the foragers of two species of stingless bees over 6 months in the Budongo Forest (March–August 2002).

Figure 3. Effect of the time of day (local time) on the sugar concentration of nectar collected by the foragers of two species of stingless bees polled together over 6 months in the Budongo Forest (March–August 2002). nectar with significantly higher sugar concen- two bee species (Tab. II). The mean nectar con- tration compared to M. ferruginea (Fig. 2) centration was higher during the dry season across each of the daily sampling periods (June: 48.9 ± 10.8 and July: 47.8 ± 11.0) com- (Fig. 3). Sugar concentration increased grad- pared to the rainy season (March: 40.2 ± 10.0 ually from 0700 h in the morning to a peak at and April: 32.5 ± 9.9). There was a positive 1300 h in the afternoon and there after it de- correlation between the concentration of col- clined. lected nectar and temperature (M. ferruginea: 2-tailed, r = 0.846, N = 260, and H. gribodoi: 2 tailed, r = 0.559, N = 313, P < 0.0001 for 3.2. Main factors influencing sugar both species). concentration of collected nectar

The species of bee, colony within species, 3.3. Nectar and pollen sources month of year and the time of day when the nectar was collected all had a significant ef- By means of palynological analysis, 33 out fect on the sugar concentration of collected of the 52 nectar sources could be identified to nectar (Tab. II). There was significant differ- species level. Overall, more plants were ma- ence in monthly sugar concentration for the jor nectar sources for H. gribodoi than for Nectar sources and sugar concentration for African stingless bees 115

Table II. Nested ANOVA with the eﬀect of bee species, colonies nested within species, month of year and time of day on the sugar concentration of collected nectar. The blank spaces correspond to non-signiﬁcant results.

Source of variation df SS MS Fcal P values Bee species 1 0.1056 0.1056 88.00 ** Colonies (species) 2 0.0223 0.0111 9.25 * Month 5 4.1933 0.2097 174.00 ** Time of day 4 12.6540 0.1318 109.83 ** Month × Time of day 20 Bee species × Month 5 Bee species × Time of day 4 Bee species × Month × Time of day 20 Colony(species) × Month 10 Colony(species) × Time of day 8 Colony(species) × Month × Time of day 40 Error 1026 1.2343 0.0012 Total 1145 18.2095

Table III. Important nectar sources for two species of stingless bees in the Budongo forest over six months of observation (March–August 2002). Shading indicates the periods of foraging on the given source.

Plant species Family March April May June July August Meliponula ferruginea Acacia sp. Fabaceae Albizia sp. Fabaceae Calliandra calothyrsus Fabaceae Coffea sp. Rubiaceae Eucalyptus sp. Myrtaceae Musa sp. Musaceae

Hypotrigona gribodoi Acacia sp. Fabaceae Albizia sp. Fabaceae Bidens sp. Asteraceae Calliandra calothyrsus Fabaceae Combretum sp. Combretaceae Eucalyptus sp. Myrtaceae Musa sp. Musaceae Type 7 Unidentified Type 14 Asteraceae Type 23 Unidentified Syzigium sp. Myrtaceae Vernonia sp. Asteraceae

M. ferruginea. The two most important fam- tus sp. being one of the two major species of ilies were Fabaceae and Asteraceae. Three of Myrtaceae was collected by both stingless bee the major species of Fabaceae (Acacia sp., species. Combretaceae, Musaceae and Rubi- Albizia sp. and Calliandra calothyrsus)were aceae accounted for one major source each. collected by both H. gribodoi and M. ferrug- The families of two major types (Type 7 and inea (Tab. III). The three species of Asteraceae Type 23) could not be determined. Callian- (Bidens sp., Vernonia sp. and type 14) were dra calothyrsus was used throughout the ob- exclusively collected by H. gribodoi. Eucalyp- servation period by both stingless bee species. 116 R. Kajobe

Table IV. Number of nectar sources and Shannon- a large variety of other insects. Observations Weaver’s index of diversity for Hypotrigona gri- of flower visitation on C. calothyrsus showed bodoi and Melipona ferruginea given as average that A. mellifera was the most common visi- over the 6 months of sampling. tor while M. ferruginea was also quite common and H. gribodoi was quite rare. Among Colony Total number of plant Diversity index (H’) the bee species, A. mellifera crop content had species foraged upon the lowest mean sugar concentration (40.3 ± Meliponula ferruginea 7.9) while H. gribodoi had the highest (44.9 1181.78± 9.4; Tab. VI). The concentration of nectar 2131.67in the crop of foragers of H. gribodoi and Hypotrigona gribodoi M. ferruginea captured at the nest entrances 1242.19was similar to that of the crop content from 2292.23bees captured at flowers immediately after imbibing the nectar for an uninterrupted period (H. gribodoi: ANOVA: F = 0.92; df = 1; N = During the study period, the two stingless bee 85; P > 0.05; M. ferruginea: ANOVA: F = species collected nectar from 52 different plant 0.98; df = 1; N = 85; P > 0.05). The species species, 13 of which were shared. M. ferrug- of bee had a significant effect on the time taken inea used 27 plant species (14 exclusively) and to visit one flower (handling time) and the for- H. gribodoi used 38 plant species (25 exclu- aging speed. It was lowest for A. mellifera and sively). H. gribodoi collected nectar from a highest for H. gribodoi (One flower: Kruskal- wider range of plants species than M. ferrug- Wallis test: df = 2, N = 85, P ≤ 0.0001; Five inea. The average Shannon-Weiner index of flowers: Kruskal-Wallis test: df = 2, N = 85, diversity (H’) was higher for H. gribodoi than P < 0.0001; Tab. VI). for M. ferruginea (Tab. IV).

4. DISCUSSION 3.4. Effects of nectar source taxa on sugar concentration 4.1. Influence of bee size on sugar concentration of collected nectar The two stingless bee species shared 13 nectar sources out of which H. gribodoi col- Distinctive preferences for nectar of dif- lected 8 of higher sugar concentration than fering sugar concentrations were found for M. ferruginea (Tab. V). H. gribodoi collected the species. The smaller bee species H. gri- a significantly lower sugar concentration from bodoi (2–3 mm) preferred sugar of signifi- the plant species it shared with M. ferruginea cantly higher concentration than M. ferrug- than from sources that it used exclusively (t = inea (6 mm). If similar volumes are compared, 2.69; P = 0.015; shared sources: mean = 43; a relatively highly concentrated nectar source N = 13; exclusive sources: mean = 51; N = 6; is energetically more profitable than or com- Tab. V). Two of the nectar sources exclusively parable to a nectar source of lower concen- used by M. ferruginea had the lowest concentration (Roubik, 1989). Since we used 20 µL trations (Type 11 with 24.5% and Type 20 with capillary tubes to collect crop loads of H. gri- 29.2%). bodoi and 50 µLforM. ferruginea, it is hy- pothised that the crop load of the smaller bee, H. gribodoi was also smaller. Probably if all 3.5. Nectar collection from Calliandra factors were kept constant (e.g. weather con- calothyrsus by stingless bees and ditions, distance to food source), the energy Apis mellifera saved by taking less concentrated nectar would not compensate foragers of H. gribodoi for C. calothyrsus was a major source of nec- the calorific loss. By harvesting significantly tar for the three bee species and was visited by more concentrated nectar, it is possible that Nectar sources and sugar concentration for African stingless bees 117

Table V. Sugar concentration (g/100 g) of nectar of diﬀerent botanic origin obtained from the crop of returning foragers of two stingless bee species in the Budongo forest (data collected between March and August 2002).

Plant species Hypotrigona gribodoi Melipona ferruginea t-value P value Mean N Mean N Calliandra calothyrsus 45.4 147 41.2 127 2.24 0.026 Eucalyptus sp. 48.1 129 44.3 98 3.04 0.003 Albizia sp. 44.3 82 40.2 102 2.24 0.026 Acacia sp. 49.1 76 43.2 97 2.44 0.016 Musa sp. 40.4 56 41.3 64 -1.67 0.098 Bidens sp. 46.2 45 38.4 39 3.40 0.001 Type 14 (Asteraceae) 42.1 41 39.4 9 2.45 0.018 Vernonia sp. 52.1 39 49.2 53 3.27 0.002 Syzigium sp. 39.6 28 42.3 25 2.11 0.040 Type 7 (Unidentified) 43.2 22 46.5 42 2.75 0.008 Type 23 (Unidentified) 38.2 19 37.1 8 1.76 0.091 Combretum sp. 37.8 17 32.3 11 3.61 0.001 Coffea sp. 40.3 15 41.2 6 1.44 0.166 Markhamia lutea 56.5 13 Mangifera indica 48.4 12 Ipomea sp. 54.4 9 Senna sp. 47.1 6 Carica papaya 58.2 5 Citrus sp. 45.3 3 Type11 (Unidentified) 24.5 5 Type 20 (Unidentified) 29.2 4

Table VI. Sugar concentration of the crop content,handling time and foraging speed for three species of bees gathering nectar on Calliandra calothyrsus (N = 85 for all cases; mean ± SD).

Bee species and body length Returning foragers Foragers caught at Time to visit Time to visit (measured on dry specimens) caught at nest entrance departure from flowers 1 flower 5 flowers %TDS %TDS s s A. mellifera (11 mm) 40.3 ± 7.9 4.3 ± 1.6 26.4 ± 5.1 M. ferruginea (6 mm) 41.9 ± 12.4 42.6 ± 6.8 5.2 ± 1.7 28.2 ± 4.5 H. gribodoi (2–3 mm) 44.1 ± 11.8 44.9 ± 9.4 5.5 ± 2.0 31.3 ± 4.0 foragers of H. gribodoi are able to reduce the The two bee species collected nectar with energy needed to evaporate the collected nec- a wide range of sugar concentrations suggest- tar to the normal concentration of stingless bee ing that the concentrations used partly over- honey which is about 70% (Vit et al., 2004). lapped between the species. The wide range of Roubik and Buchmann (1984) noted that even sugar concentration can be favourable to both if greatly rewarding resources are present, less bee species because it can ultimately result in rewarding ones might be preferred if the over- survival of these species in cases of adverse all amount of that resource in the patch is high environmental conditions and inadequate nec- and/or easy to forage. However, a sample size tar resources. Accessibility to nectar sources of two stingless bee species with two colonies by the bee species may have limited influence of each is far too small to enable the drawing of on the concentration of collected nectar be- general conclusions as to the importance of the cause the bee species collected nectar from size factor on the nectar selection process of plant species in the same families and shared stingless bees. some of their major nectar sources. 118 R. Kajobe

4.2. Effects of nectar and pollen source strategies of the bees to food sources may on sugar concentration of nectar probably explain the differences in diversity. In a related study (Kajobe and Echazarreta, Bees must possess a mechanism that 2005) found that workers of M. ferruginea ff can discriminate between nectars of di er- exited their nests in characteristically distinct ent sweetness to be able to collect the opti- foraging bouts suggesting that the recruit- mal sugar concentration. Other possible mech- ment methods employed may be direct lead- anisms are distinction by taste or sensitivity to ing or “piloting” (Esch et al., 1965; Esch, sugar concentration (Biesmeijer et al., 1999b). 1967; Johnson, 1987). Such recruitment trait Variation in plant species used by bee species could have led to the reduced diversity in nec- is one of the factors that explain the variation tar sources for M. ferruginea. This hypothesis in sugar concentration of bee collected nectar. needs to be tested further because there is little The two bee species shared 13 sources, some doubt that it is adaptive for a bee to occasion- of which were among their major sources. Of ally sample flowers other than those on which the total range of nectar and pollen sources it is specialising. Such behaviour may fre- used by the two species, H. gribodoi tended to quently occur in tropical habitats where hun- use plants with higher average nectar concen- dreds of flower species can be presented at one tration. Moreover, the shared nectar sources time (Roubik and Buchmann, 1984). were those that provided significantly less rich nectar. Thus the botanical origin of the nectar seems to explain only part of the differences in 4.5. Nectar collection from Calliandra the sugar harvest of the two species. calothyrsus by stingless bees and Apis mellifera 4.3. Temporal influence on sugar Despite the fact that bees might have har- concentration of collected nectar vested nectar from different flowers, there was no significant difference between the con- Another factor that may explain some of the centration of nectar harvested by foragers of variation in sugar concentration of collected H. gribodoi and M. ferruginea captured at the nectar is time of day. This study revealed that hive entrances as compared to nectar from the sugar concentration of the bee collected bees captured at flowers. This is in agree- nectar increased from early morning till 1300– ment with Roubik et al. (1995) who con- 1400 h and declined thereafter. This finding is cluded that nectar recently stored in the crop in line with the prediction that higher solar ra- of bees is not dehydrated. A. mellifera was diation causes evaporation and results in more the most common forager on C. calothyrsus. concentrated nectar in the flowers (Roubik and Such a situation could have arisen as a result Buchmann, 1984; Roubik; 1989). Sugar con- of contest competition (Milinski and Parker, centration of collected nectar varied during the 1991) during which the stingless bees are dis- months (seasons) of data collection. Monthly placed from the resource as a result of ag- changes in flowering phenology are likely to gressive behaviour of A. mellifera. Although ff produce di erences in nectar richness. With the competing stingless bees generally shared more rain and fewer sunny periods, there will the resource, M. ferruginea, was competitively be a low concentration of bee collected nec- stronger than H. gribodoi and exploited the tar. During the dry season, the wind evaporates shared resource faster. some of the water in the nectar thereby making Various sizes and shapes of bee mouthparts it more concentrated. may results in differences in rate at which they harvest nectar of differing concentration ff 4.4. Behavioural factors regulating and from di erent floral types. Such mor- ff partitioning of nectar resources phological di erences may ultimately lead to nectar resource partitioning. Apart from the The diet diversity of H. gribodoi was higher differences that floral structure enforces in than that of M. ferruginea. The recruitment regulating visitor type, resource partitioning Nectar sources and sugar concentration for African stingless bees 119 should reflect parameters of foraging success zweier Arten von Stachellosen Bienen wurde von that are dependent upon the physical proper- März bis August im Budonge Waldreservat im mit- ties of nectar and upon the bees themselves telwestlichen Uganda untersucht. Hauptsächliches Ziel war, die Einflussfaktoren der Zuckerkonzen- (Roubik and Buchmann, 1984). Comparison tration des gesammelten Nektars zu bestimmen. of the nectar intake rate of the three bee Es wurden jeweils zwei natürliche Nester von Hy- species shows that the larger bees tended to potrigona gribodoi und Meliponula ferruginea ge- harvest nectar faster. Fast foragers, which sug- nutzt. Einmal pro Woche wurden zu 5 verschie- gest higher nectar intake rate, collected more denen Tageszeiten Nektarproben von 10 zurück- kehrenden Sammlerinnen genommen. Ein weiteres dilute nectar. By imbibing more dilute nectar . Experiment zur Bestimmung möglicher Änderun- at a faster rate, foragers of A mellifera may gen der Konzentration des Honigmageninhalts zwi- have reached a balance between foraging en- schen den besammelten Blüten und der Rückkehr ergetics and profit. zum Nest wurden an der Stachellosen Biene Cal- Based on these results, it is concluded that liandra calothyrsus unternommen. In dieses Expe- riment wurden auch Honigbienen eingeschlossen. the botanic origin of the nectar, preference for Einmal pro Woche wurden 5 mal pro Tag Nektar- certain sugar concentration, local environmen- proben von 2–5 Sammlerinnen jeder Bienenart ge- tal conditions, temporal influences and colony nommen. recruitment behaviour may be used to explain Der von den beiden Stachellosen Bienen gesammel- part of the variation in sugar concentration of te Nektar umfasste eine weite Spanne unterschiedlicher Zuckerkonzentrationen (H. gribodoi: 14,2– the nectar collected. Other factors (not tested 67,4 %; M. ferruginea: 9,1–63,4 %; Tab. I). H. gri- in this study) that may influence sugar concen- bodoi sammelte zu jeder der untersuchten Tageszei- tration of the nectar collected include distance ten Nektar mit signifikant höherer Zuckerkonzen- of flowers from a bee nest, the number and tration als M. ferruginea (Abb. 2, 3). Die Zucker- arrangement of available flowers, floral mor- konzentration nahm vom Morgen bis zum Spitzen- wert am Nachmittag zu und nahm dann wieder ab. phology, and the willingness of nest mates to Die Bienenart, die Kolonie innerhalb der Spezies, accept nectar from a returning forager (Roubik der Jahresmonat und die Tageszeit, zu der Nektar and Buchmann, 1984; Roubik et al., 1995). gesammelt wurde, hatten alle einen signifikanten Effekt auf dessen Zuckerkonzentration (Tab. II). Von den 52 besammelten Nektarquellen wurden 33 ACKNOWLEDGEMENTS bis zur Art bestimmt. H. gribodoi nutzte 38 Pflan- zenarten, M. ferruginea 27. Beide Bienenarten hat- I am grateful to the British Ecological Society ten 13 Nektarquellen gemeinsam (Tab. V). C. ca- (BES) and the Faculty of Forestry and Nature Con- lothyrsus war für drei Bienenarten die Hauptquel- servation, Makerere University for funding this re- le (Apis mellifera, H. gribodoi und M. ferruginea), search. I especially thank Dr. J.R.S. Kaboggoza and hierbei war A. mellifera der häufigste Besucher. Professor J. Obua for their support. I am grateful to Der Honigblaseninhalt von A. mellifera wies die niedrigste mittlere Zuckerkonzentration auf (40,3 ± Dr. David W. Roubik who confirmed the identity of 7,9), bei H. gribodoi war sie am höchsten (44,9 ± the stingless bee species. I also thank the Royal Mu- 9,4; Tab. VI). Die Nektarkonzentration in der Ho- seum for Central Africa, Tervuren, in Belgium who nigblase von am Nesteingang gefangenen H. gribo- sponsored me to study their bee collection in June doi und M. ferruginea warähnlichzudervonan 2003. Blüten abgefangenen Bienen. Der weite Bereich von Zuckerkonzentrationen Origine botanique et concentration en sucres du kann ultimativ zu einer Auslese dieser Arten bei nectar récolté par deux abeilles sans aiguillon schlechten Umgebungsbedingungen oder ungeeig- dans une forêt pluviale tropicale africaine. neten Nektarquellen führen. Es wurden klare Be- vorzugungen für Nektare unterschiedlicher Zucker- konzentrationen gefunden. Möglicherweise können concentration en sucres / nectar / plante nec- H. gribodoi / / Sammlerinnen von durch das Sammeln tarifère comportement de butinage abeille von höher konzentriertem Nektar die zur Verdun- sans aiguillon / Apidae / Calliandra calothyrsus stung des gesammelten Nektars bis zu der für Sta- / Ouganda chellose Bienen normalen Konzentration von 70 % benötigte Energie reduzieren. Das Ansteigen der Zusammenfassung – Botanische Herkunft und Zuckerkonzentration des von den Bienen gesam- Zuckerkonzentration des Nektars, gesammelt in melten Nektars vom Morgen bis zum Nachmit- einem afrikanischen Regenwald von zwei Ar- tag stimmt mit der Vorhersage überein, dass die ten der Stachellosen Bienen. Das Nektarsammeln durch die höhere Sonneneinstrahlung verursachte 120 R. Kajobe

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